The cryptonephridial/rectal complex: an evolutionary adaptation for water and ion conservation.

Abstract

Arthropods have integrated digestive and renal systems, which function to acquire and maintain homeostatically the substances they require for survival. The cryptonephridial complex (CNC) is an evolutionary novelty in which the renal organs and gut have been dramatically reorganised. Parts of the renal or Malpighian tubules (MpTs) form a close association with the surface of the rectum, and are surrounded by a novel tissue, the perinephric membrane, which acts to insulate the system from the haemolymph and thus allows tight regulation of ions and water into and out of the CNC. The CNC can reclaim water and solutes from the rectal contents and recycle these back into the haemolymph. Fluid flow in the MpTs runs counter to flow within the rectum. It is this countercurrent arrangement that underpins its powerful recycling capabilities, and represents one of the most efficient water conservation mechanisms in nature. CNCs appear to have evolved multiple times, and are present in some of the largest and most evolutionarily successful insect groups including the larvae of most Lepidoptera and in a major beetle lineage (Cucujiformia + Bostrichoidea), suggesting that the CNC is an important adaptation. Here we review the knowledge of this remarkable organ system gained over the past 200 years. We first focus on the CNCs of tenebrionid beetles, for which we have an in-depth understanding from physiological, structural and ultrastructural studies (primarily in Tenebrio molitor), which are now being extended by studies in Tribolium castaneum enabled by advances in molecular and microscopy approaches established for this species. These recent studies are beginning to illuminate CNC development, physiology and endocrine control. We then take a broader view of arthropod CNCs, phylogenetically mapping their reported occurrence to assess their distribution and likely evolutionary origins. We explore CNCs from an ecological viewpoint, put forward evidence that CNCs may primarily be adaptations for facing the challenges of larval life, and argue that their loss in many aquatic species could point to a primary function in conserving water in terrestrial species. Finally, by considering the functions of renal and digestive epithelia in insects lacking CNCs, as well as the typical architecture of these organs in relation to one another, we propose that ancestral features of these organs predispose them for the evolution of CNCs.